Concerted cis-trans Interactions Fine-Tune Aluminum Tolerance

Abstract

The trivalent form (Al3+) of aluminum (Al), an abundant metal in the Earth's crust, is highly toxic to plant cells when released into soils under acidic conditions. Because approximately 50% of the world's arable soils are acidic, Al toxicity poses a big threat to crop production worldwide. Physiologically, Al toxicity inhibits root growth, leading to poor ion and water uptake by roots. Over long-term evolution, many plants have developed certain strategies to tolerate Al toxicity. One well-characterized mechanism in several species such as wheat, sorghum, and maize involves root exudation of organic acids such as citrate and malate that bind Al to form nontoxic complexes and prevent its entrance into cells. SbMATE is a root citrate transporter identified from sorghum, which confers Al tolerance via root citrate exudation into soils (Magalhaes et al., 2007Magalhaes J.V. Liu J. Guimaraes C.T. Lana U.G. Alves V.M. Wang Y.H. Schaffert R.E. Hoekenga O.A. Pineros M.A. Shaff J.E. et al.A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum.Nat. Genet. 2007; 39: 1156-1161Crossref PubMed Scopus (555) Google Scholar). While SbMATE expression is highly correlated with sorghum Al tolerance, intriguingly, introgression of the SbMATE-containing locus into Al-sensitive sorghum lines results in reduced SbMATE expression and decreased Al tolerance (Melo et al., 2013Melo J.O. Lana U.G. Pineros M.A. Alves V.M. Guimaraes C.T. Liu J. Zheng Y. Zhong S. Fei Z. Maron L.G. et al.Incomplete transfer of accessory loci influencing SbMATE expression underlies genetic background effects for aluminum tolerance in sorghum.Plant J. 2013; 73: 276-288Crossref PubMed Scopus (25) Google Scholar). In a recent study, Melo et al., 2019Melo J.O. Martins L.G.C. Barros B.A. Pimenta M.R. Lana U.G.P. Duarte C.E.M. Pastina M.M. Guimaraes C.T. Schaffert R.E. Kochian L.V. et al.Repeat variants for the SbMATE transporter protect sorghum roots from aluminum toxicity by transcriptional interplay in cis and trans.Proc. Natl. Acad. Sci. U S A. 2019; 116: 313-318Crossref PubMed Scopus (21) Google Scholar addressed the underlying genetic regulatory mechanism and found that variation in SbMATE expression is regulated both by cis elements in its promoter region and two trans-acting transcription factors encoded by genes located at a different chromosome from SbMATE. By generating near-isogenic lines and comparing SbMATE expression in different genetic backgrounds, the authors first found that allele-specific SbMATE expression is subjected to trans regulation by trans-acting factors whose favorable alleles are derived from Al-tolerant sorghum lines. Subsequently, through expression-QTL (eQTL) mapping and genome-wide association study (GWAS), they revealed that SbMATE expression is controlled by a major eQTL colocated with SbMATE on chromosome 3 and a minor eQTL on chromosome 9 in a dual manner. SbMATE promoters from different sorghum lines contain a varied number of so-called MITE repeat in which the 243-bp MITE transposable element is flanked by 20-bp and 100-bp sequences. The authors showed using yeast one-hybrid and ChIP assays that two transcription factors SbWRKY1 and SbZNF1 encoded by the genes within minor eQTL on chromosome 9 could trans-activate multiallelic SbMATE promoters through binding MITE repeats (Figure 1). The number of MITE repeats correlates with SbWRKY1 and SbZNF1 transactivation activity and likely also SbMATE expression. Consistent with this, haplotype analyses using an RIL (recombinant inbred line) population showed that homozygous Al-tolerant alleles for both SbWRKY1 and SbZNF1 exhibit the highest SbMATE expression. Interestingly, they also found that SbWRKY1 and SbZNF1 from Al-tolerant and -sensitive lines display different responses to Al3+: their expression is significantly increased in Al-tolerant lines but decreased in Al-sensitive lines. Similar to SbMATE, both SbWRKY1 and SbZNF1 showed Al-induced, time-dependent expression in root apices, further supporting that they regulate SbMATE expression. This work uncovers a sophisticated mechanism of transcriptional interplay between cis- and trans-acting factors that precisely control SbMATE expression in sorghum response to Al availability. Fine-tuning the cis-trans interactions and SbMATE or its homologous gene expression provides potential new strategies for enhancing plant Al tolerance and crop yield on acidic soils.